Deep-Sea Research II 65-70 (2012) 173–183
Contents lists available at SciVerse ScienceDirect
Deep-Sea Research II
journal homepage: www.elsevier.com/locate/dsr2
Physical and biochemical properties of the euphausiids Thysanoessa inermis,
Thysanoessa raschii, and Thysanoessa longipes in the eastern Bering Sea
H. Rodger Harvey a,n, Rachel L. Pleuthner a, Evelyn J. Lessard b, Megan J. Bernhardt b, C. Tracy Shaw c
a
Department of Ocean, Earth and Atmospheric Sciences, Old Dominion University, Norfolk, VA 23529, USA
School of Oceanography, University of Washington, Seattle, WA 98195, USA
c
Hatfield Marine Science Center, Oregon State University, Newport, OR 97365, USA
b
a r t i c l e i n f o
abstract
Available online 9 February 2012
Euphausiids are an integral part of the Bering Sea ecosystem, linking primary production to upper level
trophic levels as both consumers and prey. Species native to this region extend over a range of
geographic provinces and serve as a critical component of the movement of energy through the food
web. As one facet of the BEST-BSIERP Bering Sea program, we determined the proximate composition
and essential allometric relationships of multiple species of euphausiids collected over three years in
the eastern Bering Sea. Three euphausiid species were examined: Thysanoessa inermis, Thysanoessa
raschii, and Thysanoessa longipes. While the three species were similar with respect to size, T. inermis
had the highest average wet and dry weights per size class, as well as highest carbon and caloric
concentrations. Among the three species, T. inermis and T. longipes had similar lipid concentrations, with
T. longipes showing higher average lipid concentrations. Empirical equations were developed to
describe fundamental relationships between length, weight, PC/PN, and calorie and lipid content for
the three species over the full range of sizes encountered in the study area. Such relationships increase
our understanding of how euphausiids contribute to the carbon budget and energy input in the eastern
Bering Sea system and help to define realistic parameters for ongoing and future modeling efforts.
& 2012 Elsevier Ltd. All rights reserved.
Keywords:
Euphausiid
Lipid
Length–weight
Energy content
Carbon
Krill
1. Introduction
Euphausiids are an important component of the zooplankton
community, particularly in high latitude ecosystems such as the
Bering Sea. They are prey for many species, including commerciallyimportant fish, seabirds, and whales (Byrd et al., 1997; Cianelli et al.,
2004; Dwyer et al., 1987; Hewitt and Lipsky, 2008; Hunt et al., 1988;
Moss et al., 2009; Shuntov et al., 2000; Smith, 1991). Three euphausiids – Thysanoessa raschii, Thysanoessa inermis, and Thysanoessa
longipes – are the most abundant euphausiid species in the Bering
Sea (Pinchuk and Coyle, 2008) and play an important role in energy
transfer from lower to higher trophic levels. Among these species, T.
inermis and T. raschii are more cosmopolitan and have
been found at high latitudes throughout the northern hemisphere
(Mauchline and Fisher, 1969). T. longipes has been documented
primarily in the Japan, Okhotsk, and Bering Seas (Iguchi and Ikeda,
2005), but can be found as far north as the Arctic Ocean and as
far south as 401N, in the eastern Pacific (Boden et al., 1955; and
references therein). This paper is a contribution to the BEST-BSIERP
n
Corresponding author.
E-mail address: [email protected] (H.R. Harvey).
0967-0645/$ - see front matter & 2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.dsr2.2012.02.007
Bering Sea Project where collaborative efforts across multiple trophic
levels explored the linkages and interactions in the Eastern Bering
shelf, the context of the current physical environment, and the
potential for future climate impacts (Wiese et al., 2012).
Within the Bering Sea, these three species tend to segregate by
oceanic habitat. T. raschii are generally found on the continental shelf
in waterso100 m, while T. inermis are typically found in the midrange of water depths ( 150–200 m) and show a more polar
distribution (Lindley, 1980). T. longipes are more common in deeper
shelf, slope, and pelagic waters (4200 m) (e.g. Pinchuk and Coyle,
2008; Smith, 1991) and have been found at depths up to 500 m in the
Sea of Japan (Iguchi and Ikeda, 2004). There also appear to be
interspecific differences in diet based on studies of these species in
other regions which vary with location and season. In the boreal and
Arctic regions of the North Atlantic, T. raschii is considered omnivorous and T. inermis believed to be mainly herbivorous, but with
omnivorous tendencies (Båmstedt and Karlson, 1998; Falk-Petersen
et al., 2000; Saether et al., 1986). Both species appear to be
omnivorous during periods of food scarcity and while overwintering
(Corkett and McLaren, 1979; Mauchline and Fisher, 1969; Nemoto,
1966). It is suspected that T. inermis and T. raschii also exploit detrital
sources during sparse times (Falk-Petersen et al., 1981). The main
dietary sources of T. longipes are not well known, but Iguchi and Ikeda
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H.R. Harvey et al. / Deep-Sea Research II 65-70 (2012) 173–183
(2005) observed that lab-reared animals from the Japan Sea would
not feed on Phaeodactylum tricornutum, but did consume a diet of
Artemia nauplii supplemented with Isocrysis sp. Variation in diets of
these three species in the eastern Bering Sea during spring and
summer and their trophic responses were also examined as part of
the BEST-BSIERP Bering Sea project, but will be reported elsewhere.
There is a growing body of work on the physical attributes
(length and weight) and proximate composition (carbon and
nitrogen content; caloric content; lipid) of these three euphausiid
species in different regions of the northern hemisphere. Hopkins
et al. (1978) conducted extensive compositional measurements in
the springtime and Falk-Petersen (1981) examined seasonal and
interannual biochemical shifts for T. inermis, T. raschii, and
Meganyctiphanes norvegica in Balsfjorden, Norway. Percy and
Fife (1981), Iguchi and Ikeda (2005), Ikeda (1972), and Nomura
and Davis (2005) have also contributed measures of fundamental
properties for these three species. Specific studies have examined
variations in lipid class with respect to winter (Sargent and FalkPetersen, 1981), and seasonal change in total lipid and its
constituents throughout the Trondheim, Bals, and Ulls Fjords
(Saether et al., 1986). For T. longipes, in the Japan Sea, body
allometry, weights, carbon, nitrogen, hydrogen, and ash measurements have been made (Iguchi and Ikeda, 2005).
Given the important role of euphausiids in high latitude
ecosystems, proximate composition and length/weight relationships are needed. Several have been developed for T. inermis
(Dalpadado and Skjoldal, 1991; Falk-Petersen, 1985; Kulka and
Corey, 1982; Lindley, 1978; Matthews and Hestad, 1977;
Sameoto, 1976) and for T. raschii (Sameoto, 1976; Falk-Petersen,
1985; Lindley, 1978; Vidal and Smith, 1986) in the Northern
hemisphere (Siegel and Nicol, 2000). Kim et al. (2009) recently
developed such relationships for T. longipes in the Oyashio region.
Initial relationships describing lipid class concentration and total
length were developed by Saether et al. (1986) for M. norvegica, T.
inermis, and T. raschii collected in Norway. To our knowledge, no
systematic study on the allometric relationships and chemical
characteristics of eastern Bering Sea euphausiids has been
reported.
Proximate composition studies can examine either individual
euphausiids or composite samples. Typically, composite euphausiid
samples are sorted by species, followed by other parameters such as
sex, developmental stage, or location (e.g. Falk-Petersen et al., 1999;
Mayzaud et al., 2003; Saether et al., 1986), but rarely by length. Yet
size can be an influential factor in feeding habits (Hop et al., 2006),
growth (Dalpadado and Ikeda, 1989; Falk-Petersen, 1985; Hopkins
et al., 1984; Pinchuk and Coyle, 2008; Pinchuk and Hopcroft, 2007)
and total lipid and lipid class (Mayzaud et al., 2003). Additionally,
multiple measurements from a single composite sample are uncommon. If multiple measurements are taken from species-sorted
composite samples, sex is not taken into account and individuals
are very loosely sorted by size (Saether and Mohr, 1987; Saether
et al., 1986). This study highlights the importance of allometry in
proximate composition analyses in each of the three study species
and focuses on creating a more complete analysis of each size class
by taking multiple types of measurements from each different
composite sample. Here, multiple chemical and physical characteristics of the three euphausiid species were measured throughout the
spring/summer seasonal transition and among years. Fundamental
relationships for euphausiid wet and dry weight, carbon, nitrogen,
caloric and lipid composition using allometric measures were
determined, and a series of equations to relate these characteristics
across various size classes in the eastern Bering Sea developed.
Understanding how these values differ among these three species
provides a starting point for deciphering of how euphausiid proximate composition might respond to the dynamic Bering Sea
environment.
2008
60°
-170° -175° 180°
175°
170°
165°
160°
(A)
62°
123
40
110
58°
56°
60°
96
89
58°
54°
56°
52°
54°
52°
-175°
2009
60°
180°
175°
-170° -175° 180°
(B)
25
175°
165°
170°
160°
165°
160°
147 98 93
37
112
62°
122 104
23 115 76 177
60°
116
58°
170°
56°
43
16
68
51
54°
30
56°
9
26
52°
58°
54°
52°
-175°
2010
60°
180°
175°
-170° -175° 180°
(C)
170°
175°
31
54°
165°
160°
118
53
96
163
168
56°
170°
160°
62°
156
58°
165°
170
66
178
24
13
57
27
52°
60°
58°
33
71
24
19
56°
7
54°
52°
-175°
180°
175°
170°
165°
160°
Fig. 1. Coordinates for euphausiid sampling locations in years (A) 2008, (B) 2009,
and (C) 2010. Station numbers associated with each tow are noted near each point.
Refer to station names to identify which stations were revisited with season
shown as
spring or
summer (Google Earth, 2010).
2. Methods
2.1. Sampling locations
The study region spanned 55.28–62.251N and 164.06–178.911W
(see Fig. 1 for station locations). Stations used for analysis were
chosen based on the available length ranges and species of euphausiids obtained in night tows at those locations for each spring
and summer season. Detailed information (station coordinates, tow
type and depth, etc.) regarding collections associated with each
H.R. Harvey et al. / Deep-Sea Research II 65-70 (2012) 173–183
composite sample can be found in Appendix A. It should be noted
that the study period comprised three of the coldest and highest ice
extent years since 2001 (Stabeno et al., 2012).
2.2. Sampling procedures
Euphausiids were collected during six cruises in the spring
and summer of 2008, 2009 and 2010 (see Fig. 1, and Wiese et al.,
2012). Spring cruises took place between early April and mid-May
in 2008 and 2009; in 2010, the spring cruise was delayed until
mid-May and ended in mid-June. Summer cruises were conducted between June and late July. In 2008 and 2009, euphausiids
were collected using a 70 cm bongo net, with 333 mm mesh. The
net was towed obliquely, except in heavy ice conditions or rough
weather when vertical deployments were used. Krill were collected using several nets in 2010: a 1 m ring net with 200 mm
mesh, a 60 cm bongo net with 333 mm mesh, and a 1 m2
MOCNESS equipped with black, 505 mm mesh nets (e.g. Wiebe
and Benfield, 2003). Immediately upon recovery, euphausiids
were removed from cod ends, transferred into containers of
ambient filtered sea water, and held in the dark until sorted.
Net tows were conducted to catch krill in good condition for use
in live experiments. These tows were neither quantitative nor
designed to serve as a source of data on zooplankton distribution
or abundance. Data on distribution and abundance of zooplankton
were collected as a different component of the BEST project.
Total length determination followed that of Shaw et al. (2010)
using species-specific body length (BL) to total length (TL) conversions based on measurements made during the BEST cruises.
The species-specific equations for conversion of adult BL to TL as
defined by Mauchline (1981) for the three species are as follows:
T. raschii TL¼1.1887 BLþ0.6838 (n¼530, r2 ¼0.99).
T. inermis TL¼1.15325 BLþ0.9846 (n¼248, r2 ¼0.99).
T. longipes TL¼1.2408 BL þ0.3308 (n ¼186, r2 ¼0.99).
Euphausiids were measured with the aid of a dissecting
microscope and then sorted by species and size. Additional details
of the condition of each euphausiid were also recorded, including
sex, reproductive state (gravid, blue ovary, presence of spermatophores etc.), and presence of parasites. Heavily parasitized
animals were not used. All composite samples were binned in
2 mm TL increments to allow detailed comparisons and comprised animals at similar reproductive states whenever possible.
Krill were frozen at 80 1C either individually or as composite
samples (ranging from 2 to 50 animals depending on length) and
stored at 70 1C until analysis.
2.3. Wet and dry weights, PC/PN, and caloric content
In the laboratory, individual euphausiids were thawed, rinsed
briefly with deionized water to remove salts, blotted to remove
excess moisture, and weighed. Samples were then immediately
lyophilized overnight with a Virtis DBT 7.0 model freeze dryer
and dry weights obtained. For T. inermis and T. raschii, measures of
carbon and nitrogen content, calories, and total lipid were
performed using composite samples at 2 mm size increments
over the range of 8–28 mm (10 subsets). For T. longipes, all
proximate measurements were obtained from 2010 collections
when adequate numbers were present. Immediately prior to CHN
or calorimetric analysis, euphausiids were homogenized by grinding with a Teflon-coated pestle. PC/PN determination utilized
standard combustion methods employing a CE-440 Elemental
Analyzer with atropine serving as the standard. Caloric content
was determined with a Parr 1109 semi-micro oxygen bomb
calibrated with benzoic acid pellets. Krill were prepared using
175
the Parr 2812 Pellet Press; masses and non-combustible products
were measured to calculate gross heat (cal/g) based on ash-free
dry weight (AFDW). Ash was calculated as the percentage of
remaining dry weight. Limited sample mass confined the number
of caloric measurements to composite samples and thus values
represent average composition of krill within each 2 mm size bin.
Relative standard deviation of gross heat was 5–7% based on
replicate measurements of unsorted euphausiid composites.
2.4. Lipid extraction and analyses
Total solvent-extractable lipid isolation employed microwaveassisted solvent extraction (MASE) using a MARS5 microwave digestion system. All glassware and Teflon parts were solvent-rinsed and/
or combusted prior to use. Pre-weighed samples were transferred to
glass test tubes and extracted with 30 mL of 2:1 dichloromethane:
methanol solution at 80 1C for 30 min with an initial 4 min temperature ramp and a programmed cool down period of 5 min. Power was
set at 1600 W. After cooling below 40 1C, lipid extracts were
transferred to flasks and evaporated to dryness using rotary evaporation. Individual lipid samples were then re-dissolved in a small
volume of the extraction solvent and filtered through combusted
quartz wool to remove cellular debris. Both of these steps were
repeated twice more to ensure complete transfer. Total lipids and
major lipid classes were determined by thin-layer chromatography
with flame ionization detection (TLC–FID) using an Iatroscan MK-V
Analyzer (e.g., Harvey and Patton, 1981; Ju and Harvey, 2004).
Aliquots of total extracts were spotted onto replicate S-III Chromarods, solvent focused, and total lipids determined. Integrated peak
areas (HP ChemStation) were quantified using a calibration curve
consisting of a standard mixture of lipid classes approximating
euphausiid composition. Overall precision for total lipid and major
classes was 710% or better for replicates. For major lipid classes,
extracted lipids were developed in hexane:diethyl ether:formic acid
(85:15:0.2), which allowed individual neutral lipids to be separated in
a single development; phospholipids remained at the origin and were
not identified individually. Lipid classes were identified and calibrated
using a mixture of commercial standards (phosphatidyl choline for
phospholipids (PL), cholesterol for sterols (ST), nonadecanoic acid for
free fatty acids (FFA), triolein for triacylglycerol (TAG), and palmityl
stearate for wax esters (WE); Sigma Co.). Peak areas were quantified
using individual class calibrations, developed in tandem, of the
standard lipid mix as above.
2.5. Statistical analyses
Regression equations for paired parameters for each species in each season and year were determined using Sigma Plot
(ver. 8.0, Systat Software). To determine differences between
seasons and years both within and among species, tests for
significant differences in slopes and elevations of the regressions were made using a Student t-test or ANCOVA as outlined
in Zar (1999).
3. Results
Individual and composite samples of each species were collected
during all cruises whenever available and both seasonal and annual
collections were compared where possible. In 2009 and 2010, adequate numbers of T. inermis and T. raschii allowed evaluation of both
the spring and summer seasons, with animals collected during the
summer of 2008 included for comparison. The collection of T. longipes
in 2010 provided enough data to compare both seasons. While the
summer of 2009 provided a sufficient number of samples, the spring
of 2009 did not. Similarly, these samples were still included for
176
H.R. Harvey et al. / Deep-Sea Research II 65-70 (2012) 173–183
comparison. Significant relationships were found among all eight sets
of paired parameters, which describe important physical and biochemical properties. The empirical relationships determined for the
three species are shown in Table 1. Detailed descriptions of the trends
observed and intra- and inter-species statistical comparisons are
presented in the sections below. Average values for composite
Table 1
Equations describing the relationships between euphausiid physical and chemical properties observed in the Bering Sea. Abbreviations include: wet weight (WW); dry
weight (DW); carbon (C); nitrogen (N); and energy (E). Energy is measured in cal individual 1 and average total length is measured in mm. All other variables are
measured in units of mg individual 1.
Relationship
Field years
Species
Equation
R2
P
Regression
comparison
Graph
reference
Wet weight and total length
2008–2010
2008–2010
2009–2010
T. inermis
T. raschii
T. longipes
WW ¼0.012 TL(2.98)
WW ¼0.009 TL(3.02)
WW ¼0.009 TL(3.06)
0.97
0.95
0.99
o 0.0001
o 0.0001
o 0.0001
1
6a
Dry weight and wet weight
2008–2010
2008–2010
2009–2010
T. inermis
T. raschii
T. longipes
DW ¼ 0.239 WW(1.048)
DW ¼ 0.270 WW(0.965)
DW ¼ 0.109 WW(1.189)
0.93
0.96
0.96
o 0.0001
o 0.0001
o 0.0001
2
6b
Carbon and dry weight
2008–2009
2008–2009
2010
T. inermis
T. raschii
T. longipes
C ¼ 0.448 DW(1.079)
C ¼ 0.448 DW(1.024)
C ¼ 0.341 DW(1.130)
0.99
0.99
1.00
o 0.0001
o 0.0001
o 0.0001
3
6c
Nitrogen and dry weight
2008–2009
2008–2009
2010
T. inermis
T. raschii
T. longipes
N ¼ 0.1212 DW(0.823)
N ¼ 0.0997 DW(0.988)
N ¼ 0.1596 DW(0.774)
0.86
0.95
0.96
o 0.0001
o 0.0001
o 0.0001
4
6d
Carbon and total length
2008–2009
2008–2009
2010
T. inermis
T. raschii
T. longipes
C ¼ 0.0029 TL(2.87)
C ¼ 0.0014 TL(2.93)
C ¼ 0.000012 TL(4.64)
0.71
0.69
0.90
o 0.0001
o 0.0001
o 0.0001
5
6e
Lipid and dry weight
2009
2009
2010
T. inermis
T. raschii
T. longipes
L ¼ 0.409 DW(0.964)
L ¼ 0.453 DW(0.758)
L ¼ 0.292 DW(1.11)
0.91
0.78
0.95
o 0.0001
0.001
o 0.0001
6
6f
Energy and dry weight
2009
2009
T. inermis
T. raschii
E ¼ 4.44 DW(1.10)
E ¼ 4.81 DW(1.02)
0.98
0.97
o 0.0001
o 0.0001
7
6g
Energy and carbon
2009
2009
T. inermis
T. raschii
E ¼ 12.90 C(0.963)
E ¼ 10.08 C(1.03)
1.00
1.00
o 0.0001
o 0.0001
8
6h
1, 3, 5–8¼ slopes not statistically different when all data pooled.
2, 4 ¼slopes statistically different when all data pooled.
1, 3, 6–8¼ slopes statistically similar among all species.
2¼ slopes statistically different among all species.
4, 5 ¼slopes statistically different between T. raschii and T. longipes.
Spring
Summer
250
200
2008
150
100
50
250
200
2009
Average Wet Weight (mg)
0
150
100
50
0
250
2010
200
150
100
50
0
5
10
15
20
5
10
25
30
Average Total Length (mm)
15
20
25
30
Fig. 2. Average total length and wet weight regression for Bering Sea euphausiids. Graphs are divided by season and sampling year: (A) July, 2008 (B) April–May, 2009
(C) June–July, 2009 (D) May–June, 2010 (E) June–July, 2010. Symbols represent
T. inermis,
T. raschii, and
T. longipes.
H.R. Harvey et al. / Deep-Sea Research II 65-70 (2012) 173–183
samples were normalized to a single animal, e.g. mg C individual 1 or
average carbon content (mg C mg dry weight 1) for each parameter
among each 2 mm size bin. The relationships for each set of paired
parameters are referenced (Figs. 2–6); error bars were not shown as
177
most are smaller than the symbol area. All errors associated with each
measure are included in Appendix B. Cruise-specific data, listed in the
appendices, will be made public domain and can be accessed via the
Bering Sea Project Data Archive (http://beringsea.eol.ucar.edu/data/).
Spring
Summer
60
50
40
30
20
10
0
2009
Average Dry Weight (mg)
2008
60
50
40
30
20
10
0
2010
60
50
40
30
20
10
0
0
50
100
150
0
50
200
250
Average Wet Weight (mg)
100
150
200
250
Fig. 3. Wet versus dry weights relationship for Bering Sea euphausiids in spring and summer over the study period. Graphs are divided by season and sampling year:
(A) July, 2008 (B) April–May, 2009 (C) June–July, 2009 (D) May–June, 2010 (E) June–July, 2010. Symbols represent
T. inermis,
T. raschii, and
T. longipes.
Summer
30
25
20
15
10
5
0
10
8
6
4
2008
2
0
30
25
20
15
10
5
0
10
30
25
20
15
10
5
0
10
8
4
2009
6
2
0
Average Nitrogen content (mg)
Average Carbon content (mg)
Spring
8
4
2010
6
2
0
10
20
30
40
50
0
10
20
30
40
0
50
Average Dry Weight (mg)
Fig. 4. Average carbon and nitrogen content for Bering Sea euphausiids. Spring collections are featured on the left panel with summer on the right. Graphs are organized by
season and sampling year; (A) July, 2008 (B) April–May, 2009 (C) June–July, 2009 (D) May–June, 2010 (E) June–July, 2010. Symbols for carbon and nitrogen are shown as
’ Carbon—T. inermis,
Carbon—T. raschii,
Carbon—T. longipes, ~ Nitrogen—T. inermis,
Nitrogen—T. raschii, and
Nitrogen—T. longipes.
178
H.R. Harvey et al. / Deep-Sea Research II 65-70 (2012) 173–183
Summer
20
30
40
50
0
10
20
30
40
0
10
20
30
40
50
0
10
20
30
40
0
10
20
30
0
10
40
50
Average Dry Weight (mg)
20
30
40
300
250
200
150
100
50
0
2010
10
Average Lipid content (mg/individ)
2009
0
300
250
200
150
100
50
0
25
20
15
10
5
0
50
25
20
15
10
5
0
50
25
20
15
10
5
0
50
2009
Average Energy content (cal/individ)
Spring
300
250
200
150
100
50
0
Fig. 5. Average calorie (.) and lipid ( ) measurements for Bering Sea euphausiids during 2009 and 2010. Spring collections are shown on the left and summer on the right
for T. inermis (A, B), T. raschii (C, D), and T. longipes (E, F).
3.1. Wet weight versus total length
Wet weight increased exponentially with average total length for
all three species in spring and summer (Fig. 2). Average total lengths
for T. inermis ranged 9–23 mm during the spring and 12–23 mm in
the summer, with corresponding wet weights per individual of
7–152 mg and 16–142 mg. Average total lengths ranged 9–27 mm
during spring and 13–28 mm during summer, with average wet
weights of 7–179 mg and 18–213 mg, respectively, for T. raschii. For
T. longipes, average lengths of 10–20 mm were seen in spring with
wet weights of 6–96 mg per individual and summer lengths of
14–25 mm with wet weights of 34–185 mg. T. inermis had a higher
wet weight per unit length compared to T. raschii, except for spring
2009, and showed similar or larger wet weight per unit length
compared to T. longipes throughout the studied months. When all
cruises were combined, however, the WW:TL relationship for both T.
raschii and T. inermis show no significant differences across summed
seasons or years for each species. The few individual T. longipes
collected from the spring of 2009 precluded detailed seasonal
comparisons, but annual comparisons showed no differences. Additionally, no significant differences were noted between any of the
three species when all data were compared. Only T. longipes showed
differences within its data sets, most likely due to the sample size in
spring, 2009.
3.2. Dry weight versus wet weight relationships
When comparing T. inermis data, there were significant changes
seen among summed years, but not between the pooled seasons;
analysis of T. raschii data revealed similar results. T. longipes
exhibited opposite trend where seasons differed, but years did not.
All three species yielded significant differences when data sets were
compared within each species, as well. T. inermis generally had the
highest DW:WW, regardless of season or year (Fig. 3; Appendix B).
On average, T. raschii had the lowest wet weight for each size class,
except in the summer of 2010 when T. longipes had equal or greater
water content. T. longipes were more variable, but generally were
within the same range as the other two euphausiid species. Dry
weight with respect to size class for T. inermis was generally highest
of the three Thysanoessa species, followed by T. longipes and then
T. raschii. Comparisons among species for all data sets revealed that
each species was statistically different from the other.
3.3. Carbon and nitrogen content
The C/DW relationships within each species did not statistically
differ when all data were pooled, or when comparing between
seasons or summers, with the exception of T. raschii in the summer
seasons (2008 and 2009). Although differences were not significant
among species, T. inermis had the higher average carbon content
than T. raschii over a range of dry weights for spring and summer. T.
raschii carbon to dry weight ratios were the lowest per individual,
and those of T. longipes were intermediate (Fig. 4).
Carbon was strongly correlated with total length for all three
species (Fig. 6, Table 1), and did not statistically differ for each
species when data were pooled. No differences were seen between
seasons in the same year for T. inermis (2009) or T. longipes (2010),
unlike T. raschii. Additionally, no C:TL differences were observed
between summer data sets for T. inermis or T. raschii; T. longipes did
not have additional summer data for a comparison. Among species,
only T. raschii and T. longipes differed, statistically.
During the summer, T. raschii was generally more nitrogenrich than either T. inermis or T. longipes. On the statistical side, as
with C:DW and C:TL, pooled data within each species did not
differ. Differences between combinations of years and seasons
within each species mirrored those of the C:TL correlations.
Similarly, only differences between T. raschii and T. longipes were
noted among species.
3.4. Calories and lipids
Individual caloric and lipid content of krill showed an increase
in energy stores as the season progressed (Fig. 5). Nevertheless,
150
100
50
0
5
30
30
25
20
15
10
5
0
10
20
30
40
Average Dry Weight (mg)
50
5
10
15
20
25
Average Total Length (mg)
300
200
100
0
0
10
20
30
40
Average Dry Weight (mg)
50
0
50
100
150
200
Average Wet Weight (mg)
250
0
10
20
30
40
Average Dry Weight (mg)
50
0
10
20
30
40
Average Dry Weight (mg)
50
5
30
4.0
3.0
2.0
1.0
0.0
25
20
15
10
5
0
30
400
179
60
50
40
30
20
10
0
Lipid (mg/individ)
30
25
20
15
10
5
0
Energy (cal/individ)
Carbon (mg/individ)
0
Energy (cal/individ)
10
15
20
25
Average Total Length (mm)
Average Dry Weight (mg)
200
Nitrogen (mg/individ)
250
Carbon (mg/individ)
Average Wet Weight (mg)
H.R. Harvey et al. / Deep-Sea Research II 65-70 (2012) 173–183
400
300
200
100
0
0
10
15
20
25
Carbon (mg/individ)
Fig. 6. Regression relationships for each species with combined data from all seasons and years for length, weight, carbon, nitrogen, calories, and lipid content. Regressions are
derived from empirical equations described in Table 1. Available data for each euphausiid are listed in each panel. Symbols are shown as T. inermis, T. raschii, and T. longipes.
neither caloric concentration (as calories per gram AFDW)
nor lipid (as a percent of dry weight) had showed a consistent
relationship to size class within a species. As a general observation, T. longipes had the highest lipid content of the three species.
T. raschii were consistently within the lower range of values
measured for all three species. The high T. longipes lipid content
seen in spring may be a consequence of these krill being collected
nearly a full month later in the season as compared to the
other two species of euphausiids. Seasonal differences were not
significant between DW and lipid; DW and energy; or C and
energy between T. inermis (2009) or T. longipes (2010). Among
those three paired sets of variables, T. raschii only exhibited
seasonal differences between DW and energy.
3.5. Lipid class analysis
Lipid class analysis was performed for the largest size class of
euphausiids collected in summer 2009 (T. raschii and T. inermis) or
2010 (T. longipes) with results shown in Table 3. Phospholipids
were the dominant lipid class for all three species, with differences in types and amounts of storage lipids among species.
Wax esters, a storage class found in significant amounts within
T. inermis, were either absent or present in minor quantities in
T. raschii and T. longipes.
3.6. Empirical relationships among the three euphausiid species
The relationships observed between average total lengths and
average wet weights for each species were similar in spring and
summer seasons for all years. Interestingly, all three Thysanoessa
species had similar patterns of biomass among years (Fig. 6), but
annual changes were subtle and did not show a consistent trend.
The uniformity seen for each species across the project period
allowed each species to be represented by a single regression,
reflecting the tight correlations between length and wet weight
over multiple seasons and years (Fig. 6A). The same approach was
1
1
1
4
5b
6
5b
3
7
2008–2010
2008–2010
2009–2010
1971
1976–1977
1969
1976–1977
1997–1998
2001–2004
62.6–77.3
6.6–10.3
45.1–55.9
Data from Spring 2010 only.
Year class group-1 data.
b
a
2.2–10.7
7.1–13.4
10.9
82.2
(1) This study; (2) Hopkins et al., 1978; (3) Iguchi and Ikeda, 2005; (4) Percy and Fife, 1981; (5) Falk-Petersen et al., 1981; (6) Ikeda, 1972; (7) Nomura and Davis, 2005.
Bering Sea
Bering Sea
Bering Sea
Frobisher Bay
Balsfjorden
Bering Sea
Balsfjorden
Japan Sea
Bering Sea
35.0–53.6
14.2–31.3
36.9–50.6
52.4
40–50
7.2
35
7–13
9–13
N/A
5.9–7.4
6920–7678
5537–6835
N/A
6260–6600
66.8–75.8
72.1–81.1
66.8–80.8
68.2–79.6
5.4–7.7
6.2–11.5
6.5–8.8
50.2–62.8
41.7–53.5
47.7–55.3
Summer
T. inermis
T. raschii
T. longipes
T. inermis
T. inermis
T. raschii
T. raschii
T. longipes
T. longipes
1
1
1a
2
2
3
2008–2010
2008–2010
2010a
1977
1977
1997–1998
Bering Sea
Bering Sea
Bering Sea
Balsfjorden
Balsfjorden
Japan Sea
22.4–30.4
22.3–29.7
31.4–40.7
22.66 70.72
13.70 70.71
10–31
22–33
N/A
17.94 70.62
18.56 77.11
12.4
4353–6552
5488–6301
N/A
5241 7 349
5094 7 468
68.3–83.9
76.7–87.8
76.6–82.5
11.5–12.0
11.1–11.8
9.4–10.8
9.59 7 1.75
10.20 72.11
10.2
Field Years
Region
Lipid (% DW)
Ash (% DW)
Cal/g AFDW
43.8–45.5
40.1–42.0
42.3–47.8
43.92 7 2.81
40.64 7 4.38
43.7
The life cycles of high latitude zooplankton are strongly
influenced by the highly seasonal nature of their food supply
(Hagen and Auel, 2001, and references therein). Euphausiids that
live at high latitudes in both hemispheres commonly employ one
of several general reproductive strategies that exploit the seasonal food abundance in different ways (Falk-Petersen et al., 2000).
T. inermis builds up an abundant store of energy during the
summer phytoplankton bloom and uses it to fuel gonad maturation and reproduction starting in late winter or early spring. This
timing enables offspring to exploit the summer phytoplankton
bloom in order to build up sufficient energy reserves for overwintering. A second strategy, employed by T. raschii, is to use the
energy from the spring phytoplankton bloom to fuel reproduction directly. Since T. raschii inhabit shallower waters, they may
switch to detrital feeding during the winter as an alternate food
supply (Mauchline and Fisher, 1969; Falk-Petersen et al., 1981).
Little is known about the reproductive cycle of T. longipes, and
the information available is confined to the west Pacific subarctic
regions. The reproductive season for T. longipes – March or April
through May – overlaps with reported spring bloom periods in
Spring
T. inermis
T. raschii
T. longipes
T. inermis
T. raschii
T. longipes
4.2. Life strategies of polar euphausiids
% Water
Within the Bering Sea, euphausiids are prey to a variety
of predators, including fish like walleye pollock (Theragra
chalcogramma), various species of salmon (Brodeur et al., 2000;
Coyle et al., 2011; Tadokoro et al., 1996); seabirds (Jahncke et al.,
2005), marine mammals including whales and seals (Smith,
1991; Springer et al., 1996); and potentially squid (Ormseth
and Spital, 2010). Foraging regions of these predators differ
within the Bering Sea, and may vary for migrating species such
as whales (Smith, 1991). While the proximate composition for
krill show remarkable consistency over a range of sizes, distribution patterns of krill species have the potential to confer an
advantage on predators whose ranges overlap with the more
lipid-rich species, such as T. longipes. Pinchuk and Coyle (2008)
showed that within the Pribilof region of the Bering Sea,
T. inermis and T. longipes remained in deeper waters whereas
T. raschii stayed closer to the shelf. During recent colder years
(1999–2002), Pinchuk et al. (2008) observed that T. inermis in the
Gulf of Alaska were more abundant than subsequent years with
warmer temperatures and lower chlorophyll. Spatial separation
of krill species and differences in proximate conditions might
have implications for success of predators. The higher lipid
content of T. inermis suggests it may provide a higher quality
diet than T. raschii despite the fact that overall caloric content
was not substantially different (Fig. 5). T. longipes could also
provide a lipid-rich diet for regional predators.
% N (from DW)
4.1. Krill as a food source
% C (from DW)
4. Discussion
Species
applied to a number of other paired characteristics, including
an additional comparison of total length with carbon content
remained constant over time. The equations that describe these
important relationships, and their corresponding correlation
parameters, are described in Table 1 with their accompanying
statistical evaluation. The comparisons focus on individual species aggregated over the project period to allow the broadest
range of sizes to be evaluated; however, small subsets also show
significant differences. For example, some summer seasons were
significantly different from each other, but spring seasons were
not. Significant differences were found between species for all
WW and DW sets.
Ref.
H.R. Harvey et al. / Deep-Sea Research II 65-70 (2012) 173–183
Table 2
Major biochemical properties for euphausiids determined from this study and comparisons from other regions in the Northern Hemisphere. Spring months range from April–June and summer months from June through
September.
180
H.R. Harvey et al. / Deep-Sea Research II 65-70 (2012) 173–183
both the Oyashio Sea and the Japan Sea (Kim, 2009 and references
therein); however, it is unknown what role the bloom plays in the
accumulation of lipid by T. longipes.
These different feeding and reproductive strategies in behavior
of Bering Sea euphausiids have implications for energy transfer to
higher trophic levels. Given that euphausiids are an important
food source for a variety of species in the Bering Sea, including
nesting seabirds and commercially important fish populations,
the differences in energy content among species have potential
impacts on their predators. The observation that average caloric
and lipid content increased with season for both T. inermis and
T. raschii, suggests that both species are adequate food sources,
although T. inermis have higher carbon and calorie concentrations
per individual.
4.3. Potential impact of climate change
The similarity seen among many of the physical and biochemical properties in the three species of euphausiids over all three
years should also be viewed in light of the prevailing oceanic
conditions. After a decade of measured increases in mean annual
temperature for the eastern Bering Sea, the three field years of
this study were near or below the long term temperature mean
(Stabeno et al., 2012). As such, this study cannot directly address
potential consequences for euphausiids in a warming ocean.
Indeed, results from this study, carried out as it was under climate
conditions similar to historic conditions in the Bering Sea, may be
more applicable as baseline data for how the Bering Sea used to
be before it started warming. T. inermis is a more polar species
than T. raschii (e.g. Lindley, 1980) and an increase in ocean
temperature in the Bering Sea could shift the distribution of
T. inermis further north as they seek out their preferred water
temperature. Assuming there are predators that rely on T. inermis,
a shift in the distribution of this euphausiid in relation to
changing water temperatures could impact the distribution or
survival of predators that feed at specific locations. If such a shift
in T. inermis distribution were to occur, T. raschii is likely to be the
more locally available prey. With its more shallow water distribution and lower lipid content, it may be a lower-quality prey
item with subsequent consequences throughout the food web.
4.4. Composition comparisons of high latitude euphausiids
Results of detailed proximate analysis among the three species
of euphausiids examined here are similar to those for the same
species in other regions of the northern hemisphere (Table 2).
The majority of springtime measurements obtained from other
sources and regions fall within the range of our size-based
measurements. While %N is slightly higher for Bering Sea
T. inermis and T. raschii than seen by Hopkins et al. (1978), caloric
and lipid content are within the lower range of values measured
181
during our study. Our lipid content values are much higher, even
at the lower end of our range, than those of Nomura and Davis
(2005). Caloric content, % water and % ash measurements for
T. inermis and T. raschii from Balsfjorden, Norway fall mostly
within range observed here. For T. raschii, the lipid content found
here is much higher than that measured by Ikeda (1972) in the
Bering Sea.
The compositional similarity among euphausiids in various
regions is intriguing. Indeed, it appears that high-latitude euphausiids in both the northern and southern hemispheres have
adopted similar life history strategies (Hagen and Auel, 2001
and references therein). T. inermis shows similarities in lipid
composition and life history strategies to E. crystallorophias in
Antarctica, while T. raschii shows similarities to E. superba.
T. longipes does not have an established Antarctic congener, but
T. macrura may be a suitable alternate as both species are
omnivorous, maintain lipid stores, and contain notable quantities
of wax esters (Phleger et al., 1998; Hagen and Kattner, 1998).
T. macrura is said to exhibit some degree of carnivory; morphological characteristics, i.e. predatory arms, and observations by
Iguchi and Ikeda (2005) suggest that T. longipes could be classified
similarly (Phleger et al., 1998). T. macrura has been observed in
waters deeper than 1800 m (Falk-Petersen et al., 1999) as well as
between 120 and 220 m (Nordhausen, 1994); likewise, T. longipes
has been documented at both pelagic and epipelagic depths
(Pinchuk and Coyle, 2008).
Lipid classes for the three Thysanoessa species and their Antarctic
congeners are summarized in Table 3. For these comparisons,
relationships derived from these results are contingent on the
allometric sorting of euphausiids. Färber-Lorda et al. (2008)
assembled a suite of equations for E. superba by sorting according
to sex and developmental stage; although, they also noted that size
was also statistically significant. Mayzaud et al. (2003) observed that
for T. macrura and E. crystallorophias size was a significant factor in
relation to lipid content. Phospholipids represent an important
component of lipid storage as well as structural constituents in
sub-arctic euphausiids, which can obscure the role of lipids as
important energy reservoirs. Among the three euphausiids examined here, T. inermis show substantial stores of wax esters, not unlike
other high latitude euphausiids such as the Antarctic species E.
crystallorophias (Nicol et al., 2004). Composite samples separated by
size and sex were not feasible in the present study due to frequent
small catches of krill, yet the three euphausiid species show
predictable relationships over the entire range of sizes in this study.
There appear to be predictable patterns among multiple euphausiids
species across the high latitude oceans.
4.5. Summary
The incorporation of euphausiids into process models in the
Bering Sea and other regions is a complicated process. Different
Table 3
Lipid class comparisons, expressed as % of total lipid, of polar and sub-arctic euphausiids in Arctic and Antarctic regions.
PL
TAG
WE
ST
FFA
DAG
Total (%)
T. raschii
T. inermis
T. longipes
T. macrura (F)
E. superba
E. crystallorophias
June–July
98.3
1.3
0.2
0.2
TR
June–July
82.6
1.0
16.2
0.2
TR
June–July
85.2
11.9
2.4
0.3
0.2
Austral fall
48.5
46.1
1.6
3.3
0.5
Austral fall
43.3
4.7
49.8
1.5
0.7
100
100
100
Austral summer
45.4
ND
53
ND
1.6
ND
100
100
100
Bering Sea
this study
Bering Sea
this study
Bering Sea
this study
S. Indian Ocean
Mayzaud et al. (2003)
Marguerite Bay, Antarctica
Ju et al. (2009)
Marguerite Bay, Antarctica
Ju et al. (2009)
182
H.R. Harvey et al. / Deep-Sea Research II 65-70 (2012) 173–183
species in the same ecosystem cannot all be treated identically since
there may be considerable differences in habitat preferences, diet
preferences, timing of reproductive activity, vertical migration, etc.
(Falk-Petersen et al., 2000; Mayzaud et al., 2000; Feinberg and
Peterson, 2003; Mayzaud et al., 2003; Gómez-Gutiérrez et al., 2005;
Ju et al., 2009; Taki, 2011). The results described here allow for both
consistent and calibrated measures of major biochemical and
physical metrics for the three major Bering Sea euphausiid species,
and consequently enhance the growing body of knowledge on
their distribution and preferred habitats. Coupling this improved
information on fundamental properties with specifics of chemical
composition will contribute to increasingly accurate carbon budgets
for the Bering Sea.
5. Conclusions
Thysanoessa raschii, T. inermis and T. longipes showed remarkable consistency in proximate composition among all years of
this study. Allometric characteristics of Bering Sea euphausiids,
regardless of species, proved to be significantly correlated for a
number of physical and chemical characteristics. Lipid composition data suggest that T. raschii are dependent on the bloom to
fuel reproduction in the spring and summer, while T. inermis
appear to store energy and use it for reproduction in the late
winter or early spring. T. longipes may also exploit the bloom
when available, but lipid content suggests that their diet remains
omnivorous even during bloom conditions. Lipid composition
data also suggest that the higher WE levels in T. inermis make it
a more desirable prey item for species that are growing and
reproducing during the short productive season in the Bering Sea.
The Bering Sea Project comprised three of the coldest years in the
Bering Sea since 1998. Results presented here may be more
typical of the Bering Sea ecosystem as it was prior to extremes
in reduction of sea ice, and should be useful as a standard for
comparison with similar studies conducted during warmer years.
Acknowledgments
This work was supported by the National Science Foundation
through the Arctic Natural Sciences program to HRH and EJL as
part of the BEST program. We thank the crews of the USCGC Healy,
the R/V Knorr, and the R/V Thompson; Alexei Pinchuk for the use
of his MOCNESS; and Edward Durbin for the bongo net loan.
Virginia Engel, Karen Taylor, Eli Moore, and Jessica Faux provided
much help with sampling. Thanks also to Thomas Miller at
UMCES for use of his calorimeter and Denise Yost and Laura
Lockard for technical assistance. This is OEAS MOGEL Contribution # 11-004 of Old Dominion University and BEST-BSIERP
Contribution # 49.
Appendix A. Supplementary material
Supplementary data associated with this article can be found
in the online version at doi:10.1016/j.dsr2.2012.02.007.
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